BLM SUMOylation regulates ssDNA accumulation at stalled replication forks

Frontiers in Genetics

Volumn 4, Issue SEP, 2013, Pages

  Ouyang, Karen J ^a,d   Yagle, Mary K ^b   Matunis, Michael J ^c   Ellis, Nathan A ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bloom's syndrome; DNA repair foci; Homologous recombination; RecQ DNA helicases; Replication fork stability

Indexed keywords

EID: 84886034846     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00167     Document Type: Article

References (88)

1. Altmannova, V., Eckert-Boulet, N., Arneric, M., Kolesar, P., Chaloupkova, R., Damborsky, J., et al. (2010). Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 38, 4708-4721. doi:10.1093/nar/gkq195.
2. Balajee, A. S., and Geard, C. R. (2004). Replication protein A and gamma-H2AX foci assembly is triggered by cellular response to DNA double-strand breaks. Exp. Cell Res. 300, 320-334. doi:10.1016/j.yexcr.2004.07.022.
3. Bansbach, C. E., Bétous, R., Lovejoy, C. A., Glick, G. G., and Cortez, D. (2009). The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes Dev. 23, 2405-2414. doi:10.1101/gad.1839909.
4. Barefield, C., and Karlseder, J. (2012). The BLM helicase contributes to telomere maintenance through processing of late-replicating intermediate structures. Nucleic Acids Res. 40, 7358-7367. doi:10.1093/nar/gks407.
5. Bartos, J. D., Wang, W., Pike, J. E., and Bambara, R. A. (2006). Mechanisms by which Bloom protein can disrupt recombination intermediates of Okazaki fragment maturation. J. Biol. Chem. 281, 32227-32239. doi:10.1074/jbc. M606310200.
6. Beresten, S. F., Stan, R., van Brabant, A. J., Ye, T., Naureckiene, S., and Ellis, N. A. (1999). Purification of overexpressed hexahistidine-tagged BLM N431 as oligomeric complexes. Protein Expr. Purif. 17, 239-248. doi:10.1006/prep.1999.1135.
7. Bergink, S., and Jentsch, S. (2009). Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458, 461-467. doi:10.1038/nature07963.
8. Branzei, D., Sollier, J., Liberi, G., Zhao, X., Maeda, D., Seki, M., et al. (2006). Ubc9-and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127, 509-522. doi:10.1016/j.cell.2006.08.050.
9. Brosh, R. M. Jr., Li, J. L., Kenny, M. K., Karow, J. K., Cooper, M. P., Kureekattil, R. P., et al. (2000). Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275, 23500-23508. doi:10.1074/jbc. M001557200.
10. Burgess, R. C., Rahman, S., Lisby, M., Rothstein, R., and Zhao, X. (2007). The Slx5-Slx8 complex affects sumoylation of DNA repair proteins and negatively regulates recombination. Mol. Cell. Biol. 27, 6153-6162. doi:10.1128/MCB.00787-07.
11. Bussen, W., Raynard, S., Busygina, V., Singh, A. K., and Sung, P. (2007). Holliday junction processing activity of the BLM-Topo IIIalpha-BLAP75 complex. J. Biol. Chem. 282, 31484-31492. doi:10.1074/jbc. M706116200.
12. Byun, T. S., Pacek, M., Yee, M. C., Walter, J. C., and Cimprich, K. A. (2005). Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19, 1040-1052. doi:10.1101/gad.1301205.
13. Carreira, A., Hilario, J., Amitani, I., Baskin, R. J., Shivji, M. K., Venkitaraman, A. R., et al. (2009). The BRC repeats of BRCA2 modulate the DNA-binding selectivity of RAD51. Cell 136, 1032-1043. doi:10.1016/j.cell.2009.02.019.
14. Chaganti, R. S., Schonberg, S., and German, J. (1974). A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 71, 4508-4512. doi:10.1073/pnas.71.11.4508.
15. Chan, K. L., North, P. S., and Hickson, I. D. (2007). BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 26, 3397-3409. doi:10.1038/sj.emboj.7601777.
16. Chan, K. L., Palmai-Pallag, T., Ying, S., and Hickson, I. D. (2009). Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11, 753-760. doi:10.1038/ncb1882.
17. Chen, C. F., and Brill, S. J. (2010). An essential DNA strand-exchange activity is conserved in the divergent N-termini of BLM orthologs. EMBO J. 29, 1713-1725. doi:10.1038/emboj.2010.61.
18. Davalos, A. R., and Campisi, J. (2003). Bloom syndrome cells undergo p53-dependent apoptosis and delayed assembly of BRCA1 and NBS1 repair complexes at stalled replication forks. J. Cell Biol. 162, 1197-1209. doi:10.1083/jcb.200304016.
19. Davies, S. L., North, P. S., Dart, A., Lakin, N. D., and Hickson, I. D. (2004). Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24, 1279-1291. doi:10.1128/MCB.24.3.1279-1291.2004.
20. Davies, S. L., North, P. S., and Hickson, I. D. (2007). Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nat. Struct. Mol. Biol. 14, 677-679. doi:10.1038/nsmb1267.
21. Doherty, K. M., Sommers, J. A., Gray, M. D., Lee, J. W., von Kobbe, C., Thoma, N. H., et al. (2005). Physical and functional mapping of the replication protein a interaction domain of the werner and bloom syndrome helicases. J. Biol. Chem. 280, 29494-29505. doi:10.1074/jbc. M500653200.
22. Dou, H., Huang, C., Singh, M., Carpenter, P. B., and Yeh, E. T. (2010). Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. Mol. Cell 39, 333-345. doi:10.1016/j.molcel.2010.07.021.
23. Driscoll, R., and Cimprich, K. A. (2009). HARPing on about the DNA damage response during replication. Genes Dev. 23, 2359-2365. doi:10.1101/gad.1860609.
24. Eladad, S., Ye, T.-Z., Hu, P., Leversha, M., Beresten, S., Matunis, M. J., et al. (2005). Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum. Mol. Genet. 14, 1351-1365. doi:10.1093/hmg/ddi145.
25. Ellis, N. A., Groden, J., Ye, T. Z., Straughen, J., Lennon, D. J., Ciocci, S., et al. (1995). The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83, 655-666. doi:10.1016/0092-8674(95)90105-1.
26. Feng, Z., Scott, S. P., Bussen, W., Sharma, G. G., Guo, G., Pandita, T. K., et al. (2011). Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl. Acad. Sci. U.S.A. 108, 686-691. doi:10.1073/pnas.1010959107.
27. Feng, Z., and Zhang, J. (2012). A dual role of BRCA1 in two distinct homologous recombination mediated repair in response to replication arrest. Nucleic Acids Res. 40, 726-738. doi:10.1093/nar/gkr748.
28. Galanty, Y., Belotserkovskaya, R., Coates, J., Polo, S., Miller, K. M., and Jackson, S. P. (2009). Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939. doi:10.1038/nature08657.
29. Galanty, Y., Belotserkovskaya, R., Coates, J., and Jackson, S. P. (2012). RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195. doi:10.1101/gad.188284.112.
30. German, J. (1964). Cytological evidence for crossing-over in vitro in lymphoid cells. Science 144, 298-301. doi:10.1126/science.144.3616.298.
31. German, J., and Crippa, L. P. (1966). Chromosomal breakage in diploid cell lines from Bloom's syndrome and Fanconi's anemia. Ann. Genet. 9, 143-154. Grimme, J. M., Honda, M., Wright, R., Okuno, Y., Rothenberg, E., Mazin, A. V., et al. (2010). Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52-ssDNA complexes. Nucleic Acids Res. 38, 2917-2930. doi:10.1093/nar/gkp1249.
32. Groden, J., Nakamura, Y., and German, J. (1990). Molecular evidence that homologous recombination occurs in proliferating human somatic cells. Proc. Natl. Acad. Sci. U.S.A. 87, 4315-4319. doi:10.1073/pnas.87.11.4315.
33. Guzzo, C. M., Berndsen, C. E., Zhu, J., Gupta, V., Datta, A., Greenberg, R. A., et al. (2012). RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci. Signal. 5, ra88. doi:10.1126/scisignal.2003485.
34. Hand, R., and German, J. (1975). A retarded rate of DNA chain growth in Bloom's syndrome. Proc. Natl. Acad. Sci. U.S.A. 72, 758-762. doi:10.1073/pnas.72.2.758.
35. Heyer, W. D., Ehmsen, K. T., and Liu, J. (2010). Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44, 113-139. doi:10.1146/annurev-genet-051710-150955.
36. Karow, J. K., Chakraverty, R. K., and Hickson, I. D. (1997). The Bloom's syndrome gene product is a 3'-5' DNA helicase. J. Biol. Chem. 272, 30611-30614. doi:10.1074/jbc.272.49.30611.
37. Lambert, S., Mizuno, K., Blaisonneau, J., Martineau, S., Chanet, R., Fréon, K., et al. (2010). Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol. Cell 39, 346-359. doi:10.1016/j.molcel.2010.07.015.
38. Langlois, R. G., Bigbee, W. L., Jensen, R. H., and German, J. (1989). Evidence for increased in vivo mutation and somatic recombination in Bloom's syndrome. Proc. Natl. Acad. Sci. U.S.A. 86, 670-674. doi:10.1073/pnas.86.2.670.
39. LaRocque, J. R., Stark, J. M., Oh, J., Bojilova, E., Yusa, K., Horie, K., et al. (2011). Interhomolog recombination and loss of heterozygosity in wild-type and Bloom syndrome helicase (BLM)-deficient mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 108, 11971-11976. doi:10.1073/pnas.1104421108.
40. Li, W., Kim, S. M., Lee, J., and Dunphy, W. G. (2004). Absence of BLM leads to accumulation of chromosomal DNA breaks during both unperturbed and disrupted S phases. J. Cell Biol. 165, 801-812. doi:10.1083/jcb.200402095.
41. Liberi, G., Maffioletti, G., Lucca, C., Chiolo, I., Baryshnikova, A., Cotta-Ramusino, C., et al. (2005). Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19, 339-350. doi:10.1101/gad.322605.
42. Lönn, U., Lönn, S., Nylen, U., Winblad, G., and German, J. (1990). An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancer Res. 50, 3141-3145.
43. Lukas, C., Savic, V., Bekker-Jensen, S., Doil, C., Neumann, B., Pedersen, R. S., et al. (2011). 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253. doi:10.1038/ncb2201.
44. Luo, K., Zhang, H., Wang, L., Yuan, J., and Lou, Z. (2012). Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 31, 3008-3019. doi:10.1038/emboj.2012.158.
45. Mimitou, E. P., and Symington, L. S. (2009). Nucleases and helicases take center stage in homologous recombination. Trends Biochem. Sci. 34, 264-272. doi:10.1016/j.tibs.2009.01.010.
46. Méndez, J., and Stillman, B. (2000). Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle:assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20, 8602-8612. doi:10.1128/MCB.20.22.8602-8612.2000.
47. Mohaghegh, P., Karow, J. K., Brosh, R. M. Jr., Bohr, V. A., and Hickson, I. D. (2001). The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 29, 2843-2849. doi:10.1093/nar/29.13.2843.
48. Morris, J. R., Boutell, C., Keppler, M., Densham, R., Weekes, D., Alamshah, A., et al. (2009). The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890. doi:10.1038/nature08593.
49. Nimonkar, A. V., Ozsoy, A. Z., Genschel, J., Modrich, P., and Kowalczykowski, S. C. (2008). Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl. Acad. Sci. U.S.A. 105, 16906-16911. doi:10.1073/pnas.0809380105.
50. Nimonkar, A. V., Genschel, J., Kinoshita, E., Polaczek, P., Campbell, J. L., Wyman, C., et al. (2011). BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 25, 350-362. doi:10.1101/gad.2003811.
51. Ohuchi, T., Seki, M., Branzei, D., Maeda, D., Ui, A., Ogiwara, H., et al. (2008). Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. DNA Repair 7, 879-889. doi:10.1016/j.dnarep.2008.02.005.
52. Ouyang, K. J., Woo, L. L., Zhu, J., Huo, D., Matunis, M. J., and Ellis, N. A. (2009). SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol. 7:e1000252. doi:10.1371/journal.pbio.1000252.
53. Pâques, F., and Haber, J. E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404.
54. Petermann, E., and Helleday, T. (2010). Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 11, 683-687. doi:10.1038/nrm2974.
55. Petermann, E., Orta, M. L., Issaeva, N., Schultz, N., and Helleday, T. (2010). Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 37, 492-502. doi:10.1016/j.molcel.2010.01.021.
56. Rao, V. A., Conti, C., Guirouilh-Barbat, J., Nakamura, A., Miao, Z. H., Davies, S. L., et al. (2007). Endogenous gamma-H2AX-ATM-Chk2 checkpoint activation in Bloom's syndrome helicase deficient cells is related to DNA replication arrested forks. Mol. Cancer Res. 5, 713-724. doi:10.1158/1541-7786.MCR-07-0028.
57. Raynard, S., Bussen, W., and Sung, P. (2006). A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J. Biol. Chem. 281, 13861-13864. doi:10.1074/jbc. C600051200.
58. Rijkers, T., Van Den Ouweland, J., Morolli, B., Rolink, A. G., Baarends, W. M., Van Sloun, P. P., et al. (1998). Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18, 6423-6429.
59. Sacher, M., Pfander, B., Hoege, C., and Jentsch, S. (2006). Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 8, 1284-1290. doi:10.1038/ncb1488.
60. Saintigny, Y., Delacôte, F., Varès, G., Petitot, F., Lambert, S., Averbeck, D., et al. (2001). Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20, 3861-3870. doi:10.1093/emboj/20.14.3861.
61. Santa Maria, S. R., Gangavarapu, V., Johnson, R. E., Prakash, L., and Prakash, S. (2007). Requirement of Nse1, a subunit of the Smc5-Smc6 complex, for Rad52-dependent postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 27, 8409-8418. doi:10.1128/MCB.01543-07.
62. Schlacher, K., Christ, N., Siaud, N., Egashira, A., Wu, H., and Jasin, M. (2011). Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145, 529-542. doi:10.1016/j.cell.2011.03.041.
63. Schlacher, K., Wu, H., and Jasin, M. (2012). A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22, 106-116. doi:10.1016/j.ccr.2012.05.015.
64. Sen, D., Nandakumar, D., Tang, G. Q., and Patel, S. S. (2012). Human mitochondrial DNA helicase TWINKLE is both an unwinding and annealing helicase. J. Biol. Chem. 287, 14545-14556. doi:10.1074/jbc. M111.309468.
65. Sengupta, S., Linke, S. P., Pedeux, R., Yang, Q., Farnsworth, J., Garfield, S. H., et al. (2003). BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J. 22, 1210-1222. doi:10.1093/emboj/cdg114.
66. Sengupta, S., Robles, A. I., Linke, S. P., Sinogeeva, N. I., Zhang, R., Pedeux, R., et al. (2004). Functional interaction between BLM helicase and 53BP1 in a Chk1-mediated pathway during S-phase arrest. J. Cell Biol. 166, 801-813. doi:10.1083/jcb.200405128.
67. Sidorova, J. M., Kehrli, K., Mao, F., and Monnat, R. Jr. (2013). Distinct functions of human RECQ helicases WRN and BLM in replication fork recovery and progression after hydroxyurea-induced stalling. DNA Repair 12, 128-139. doi:10.1016/j.dnarep.2012.11.005.
68. Singh, T. R., Ali, A. M., Busygina, V., Raynard, S., Fan, Q., Du, C. H., et al. (2008). BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev. 22, 2856-2868. doi:10.1101/gad.1725108.
69. Sleeth, K. M., SØrensen, C. S., Issaeva, N., Dziegielewski, J., Bartek, J., and Helleday, T. (2007). RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J. Mol. Biol. 373, 38-47. doi:10.1016/j.jmb.2007.07.068.
70. Thorslund, T., McIlwraith, M. J., Compton, S. A., Lekomtsev, S., Petronczki, M., Griffith, J. D., et al. (2010). The breast cancer tumor suppressor BRCA2 promotes the specific targeting of RAD51 to single-stranded DNA. Nat. Struct. Mol. Biol. 17, 1263-1265. doi:10.1038/nsmb.1905.
71. Torres-Rosell, J., Sunjevaric, I., De Piccoli, G., Sacher, M., Eckert-Boulet, N., Reid, R., et al. (2007). The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923-931. doi:10.1038/ncb1619.
72. Ulrich, H. D. (2009). Regulating post-translational modifications of the eukaryotic replication clamp PCNA. DNA Repair 8, 461-469. doi:10.1016/j.dnarep.2009.01.006.
73. Vyas, R., Kumar, R., Clermont, F., Helfricht, A., Kalev, P., Sotiropoulou, P., et al. (2013). RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ. 20, 490-502. doi:10.1038/cdd.2012.145.
74. Wechsler, T., Newman, S., and West, S. C. (2011). Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 471, 642-646. doi:10.1038/nature09790.
75. Wray, J., Liu, J., Nickoloff, J. A., and Shen, Z. (2008). Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. Cancer Res. 68, 2699-2707. doi:10.1158/0008-5472.CAN-07-6505.
76. Wu, L., and Hickson, I. D. (2003). The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874. doi:10.1038/nature02253.
77. Wu, L., Bachrati, C. Z., Ou, J., Xu, C., Yin, J., Chang, M., et al. (2006). BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. U.S.A. 103, 4068-4073. doi:10.1073/pnas.0508295103.
78. Wu, Y., Kantake, N., Sugiyama, T., and Kowalczykowski, S. C. (2008). Rad51 protein controls Rad52-mediated DNA annealing. J. Biol. Chem. 283, 14883-14892. doi:10.1074/jbc. M801097200.
79. Xia, F., Taghian, D. G., DeFrank, J. S., Zeng, Z. C., Willers, H., Iliakis, G., et al. (2001). Deficiency of human BRCA2 leads to impaired homologous recombination but maintains normal nonhomologous end joining. Proc. Natl. Acad. Sci. U.S.A. 98, 8644-8649. doi:10.1073/pnas.151253498.
80. Xu, D., Guo, R., Sobeck, A., Bachrati, C. Z., Yang, J., Enomoto, T., et al. (2008). RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes Dev. 22, 2843-2855. doi:10.1101/gad.1708608.
81. Yamaguchi-Iwai, Y., Sonoda, E., Buerstedde, J. M., Bezzubova, O., Morrison, C., Takata, M., et al. (1998). Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell. Biol. 18, 6430-6435.
82. Yang, H., Li, Q., Fan, J., Holloman, W. K., and Pavletich, N. P. (2005). The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 433, 653-657. doi:10.1038/nature03234.
83. Yang, K., Moldovan, G. L., Vinciguerra, P., Murai, J., Takeda, S., and D'Andrea, A. D. (2011). Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. Genes Dev. 25, 1847-1858. doi:10.1101/gad.17020911.
84. Yin, Y., Seifert, A., Chua, J. S., Maure, J. F., Golebiowski, F., and Hay, R. T. (2012). SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196-1208. doi:10.1101/gad.189274.112.
85. Yuan, J., Ghosal, G., and Chen, J. (2009). The annealing helicase HARP protects stalled replication forks. Genes Dev. 23, 2394-2399. doi:10.1101/gad.1836409.
86. Yusufzai, T., and Kadonaga, J. T. (2010). Annealing helicase 2 (AH2), a DNA-rewinding motor with an HNH motif. Proc. Natl. Acad. Sci. U.S.A. 107, 20970-20973. doi:10.1073/pnas.1011196107.
87. Yusufzai, T., and Kadonaga, J. T. (2008). HARP is an ATP-driven annealing helicase. Science 322, 748-750. doi:10.1126/science.1161233.
88. Zhu, J., Zhu, S., Guzzo, C. M., Ellis, N. A., Sung, K. S., Choi, C. Y., et al. (2008). Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J. Biol. Chem. 283, 29405-29415. doi:10.1074/jbc. M803632200.